SUMMARY

Nowadays few people consider finding their way in unfamiliar areas a
problem as a GPS (Global Positioning System) combined with some simple map
software can easily tell you how to get from A to B. Although this opportunity
has only become available during the last decade, recent experiments show that
long-distance migrating animals had already solved this problem. Even after
displacement over thousands of kilometres to previously unknown areas,
experienced but not first time migrant birds quickly adjust their course
toward their destination, proving the existence of an experience-based GPS in
these birds. Determining latitude is a relatively simple task, even for
humans, whereas longitude poses much larger problems. Birds and other animals
however have found a way to achieve this, although we do not yet know how.
Possible ways of determining longitude includes using celestial cues in
combination with an internal clock, geomagnetic cues such as magnetic
intensity or perhaps even olfactory cues. Presently, there is not enough
evidence to rule out any of these, and years of studying birds in a laboratory
setting have yielded partly contradictory results. We suggest that a concerted
effort, where the study of animals in a natural setting goes hand-in-hand with
lab-based study, may be necessary to fully understand the mechanism underlying
the long-distance navigation system of birds. As such, researchers must remain
receptive to alternative interpretations and bear in mind that animal
navigation may not necessarily be similar to the human system, and that we
know from many years of investigation of long-distance navigation in birds
that at least some birds do have a GPS – but we are uncertain how it
works.

Introduction

Navigation is an essential part of the life of most mobile animals. Often
they have to find their way back to a nest, a burrow or some other feature on
which they are dependent. Such navigation tasks range from a few metres, e.g.
as in the case of ants, up to thousands of kilometres, e.g. as in the case of
foraging albatrosses. The scale of these tasks varies enormously and thus
different systems probably come into play. Even though the simplest navigation
tasks may rely on retracing a route or simple recognition of landscape
features, most species have other means of ensuring a safe return. In desert
ants and many mammals, the outbound path is recorded and integrated to allow
the calculation of the direction back to the origin. Such systems are probably
too unreliable over longer ranges, because errors in distance measurements are
compounded. Rather than relying on path integration, other animals are capable
of true navigation, originally described as type III homing by Griffin: `the
ability to choose approximately the correct direction to its goal when carried
in a new and unaccustomed direction'
(Griffin, 1952).

Although an ability for true navigation is thought to exist in many
species, it has actually only been shown in a few cases, especially over
longer distances (Table 1). In
general, evidence for an ability to use true navigation comes from
displacement experiments. If an animal is able to return home from unfamiliar
territory after being translocated without access to any cues during the
displacement this is evidence for such an ability. Displacement experiments
have been performed in a number of animals (for a review of bird displacement,
see Åkesson, 2003),
notably albatrosses (Kenyon and Rice,
1958) and shearwaters (Mazzeo,
1953), over thousands of kilometres and the ability is well known
in pigeons that fly back to their home lofts
(Wallraff, 2005)
(Table 1). Other more indirect
evidence for true navigation comes from studies of migratory species in which
individuals tend to converge along some travel pathway, indicating the ability
to diverge and come back (Table
1).

However, the question of how animals perform these tasks has been a subject
of intense research and debate for decades. Human navigators, having existed
long before the advent of modern GPS systems, have generally considered the
two axes: latitude and longitude. Both can be determined from the position and
movement of celestial bodies; however, determining longitude is far more
difficult than latitude (Gould,
2008). Effective determination of longitude requires access to a
clock, which is independent of the celestial bodies, and this problem was
first solved in the 18th century (Gould,
2008). Even though birds have obviously solved the problem of true
navigation, we still have limited knowledge about how this is done. This is
especially the case over longer distances far beyond the tasks performed
within the normal home range as seen in most sedentary species, e.g. homing
pigeons (Gould, 2008).
Long-range navigation, performed by billions of migrants each year finding the
way as they return to familiar breeding sites in spring and wintering sites in
autumn, will be the focus of this commentary.

Homing vs migration

Homing is the process of finding a known location. Homing can be an
important part in migratory orientation, but at least in first-time migrants
the `goal' (e.g. the species-specific winter grounds) cannot be known and thus
homing cannot be involved in first-time migration. While adult birds of most
species in general return to the same overall breeding and wintering areas
that they have previously visited, little is known about the degree to which
navigation to these areas is based on homing or whether they rely on the
inherited migration programme that originally guided them to previously
unvisited wintering grounds. However, it is most likely that at least part of
the migration process in experienced birds can be considered a homing process
(e.g. Alerstam et al.,
2006).

Homing has been intensively studied in pigeons. These animals are able to
return to a home loft from distances as far as 700 km away or even further and
this can be achieved without access to any cues during the outward journey
(Wallraff, 2005). However,
whereas in some regions the range of an individual's navigation system
probably covers more than a thousand kilometres, in many others it is likely
to cover several hundred kilometres only
(Wallraff, 2005). Given that
migratory birds make journeys of as far as 15,000 km, one way, in the 10 g
willow warbler and 19,000 km, almost from pole to pole, in the arctic tern
(Alerstam et al., 2003), this
suggests that there may be differences in the process of homing in a central
place foraging bird such as a pigeon and a migrating bird.

Three long-distance displacement experiments, two showing a difference in
orientation between experienced and inexperienced birds and one showing a
change in orientation after displacement in spring. (A) Recoveries of 11,000
starlings displaced from The Netherlands to Switzerland. The normal wintering
area of starlings captured in The Netherlands is shaded dark. Areas with
recoveries in the winter following replacement are shown for juveniles (red)
and adults (yellow). The juveniles generally continued in the normal migration
direction whereas adults flew back toward their normal wintering ground in The
Netherlands (dark shading). After Perdeck
(Perdeck, 1958). (B)
White-crowned sparrows displaced from Seattle, WA, USA, to Princeton, NJ, USA.
The map to the left shows the displacement and breeding area (green),
wintering area (cyan) and normal migration route (blue) as well as possible
migration routes [red arrows: (1) normal migration direction, (2) toward
normal winter grounds and (3) toward capture site] after release at New
Jersey. The circle to the right shows the directions with the mean and
confidence interval indicated in which adults (blue) and juveniles (red) flew
after being released in New Jersey. Adults flew in the direction toward their
normal wintering grounds whereas juveniles continued in their normal migration
direction. After Thorup et al. (Thorup et
al., 2007). (C) Reed warblers displaced from Rybachi to
Zvenigorod, Russia. The map to the left shows the displacement and possible
orientation responses after displacement [dotted arrows: (1) normal migration
direction, (2) toward normal breeding grounds and (3) toward capture site].
The circles to the right show the observed orientation with mean and
confidence interval indicated before (upper) and after (lower) displacement.
The birds clearly correct for the eastward displacement and turn their
orientation to the west. Reprinted from Chernetsov et al.
(Chernetsov et al., 2008) with
permission from Elsevier.

Two recent studies (Thorup et al.,
2007; Chernetsov et al.,
2008) highlight the extraordinary ability of experienced migratory
birds to home toward their normal wintering and breeding grounds, respectively
(Fig. 1B,C). The study by
Thorup et al. was carried out in the wild by following radio-tagged birds,
which had been translocated more than 3000 km, in a small aircraft
(Thorup et al., 2007). The
adult birds took a direction straight towards their normal wintering grounds,
showing the global nature of their navigational task. The birds flew
individually and were certainly well beyond the area that they had known
previously. In the study by Chernetsov et al., experienced migrants corrected
their orientation in cages after being displaced approximately 1000 km
(Chernetsov et al., 2008).

How navigation works

For practical reasons we will define navigation and orientation as two
separate processes (Åkesson,
2003). To successfully home from unfamiliar territory one needs to
navigate whereas orientation involves only the ability to take up a particular
direction. Thus, navigation allows correction for displacements whereas the
latter does not. This distinction is crucial in animal orientation/navigation
studies. That animals are able to follow a chosen direction has been
convincingly shown, with different studies showing that animals are able to
use both the sun (Kramer,
1953), stars (Emlen,
1967) and the geomagnetic field
(Wiltschko and Wiltschko,
1972) as compasses for orientation.

The navigational process represents an ability to locate ones position with
respect to a goal. It has been defined by Griffin
(Griffin, 1952) and more
recently by Able (Able, 2001)
as taking a number of forms but is most simply reduced to the ability to find
a goal from a familiar area or an unfamiliar area. In a familiar area, it is
presumed that cues recognised at the site of displacement from previous visits
indicate the direction to home (Holland,
2003). In the case of unfamiliar area navigation, while it is
thought that the animal also uses cues detected at the site of displacement,
it has never experienced the particular conditions or combinations of cues at
the unfamiliar site before. How and what cues animals use for unfamiliar area
navigation remain the most controversial aspect of the field and while there
are a number of theoretical constructs as to how they might be used, so far,
the way in which animals navigate from an unfamiliar area remains to be
solved.

Experienced-based navigation

In contrast to the navigational mechanisms found in experienced birds, the
principal guiding mechanisms used by first-time migrants is most probably a
simple form of orientation, where the bird reaches its wintering grounds by
flying in certain directions for certain periods of time (known as vector
navigation). Evidence for an experienced-based navigation system in migratory
birds comes from an impressive experiment carried out on starlings by Perdeck
(Perdeck, 1958). In that
study, more than 11,000 starlings caught on migration in The Netherlands were
transported to Switzerland and ringed. After release, recoveries of the adult
birds were in a north-westerly direction from the release site on the way
toward their normal wintering grounds in the south of England and in northwest
France whereas juveniles were recovered in south-westerly directions
corresponding to the normal direction of migration through The Netherlands
(Fig. 1A). The obvious
conclusion was that experienced birds homed toward their previously visited
winter grounds whereas the young, inexperienced migrants relied on an innate
one-direction compass programme.

However, the starling is a short-distance, social, diurnal migrant in which
juveniles could easily be thought to follow the migration route of local
starlings. Repeating the starling experiment on a true long-distance,
individually migrating bird did not seem feasible for many years due to the
difficulties of tracking wild birds. Finally, the experiment was `repeated' in
2007 when Thorup et al. (Thorup et al.,
2007) found a similar difference between adult and juveniles in
their study as the one found by Perdeck in white-crowned sparrows, a
long-distance, nocturnal, solitary songbird migrant
(Perdeck, 1958)
(Fig. 1B).

It is worth noting that a few studies testing the orientation in cages
indicate that the distinction may not be that clear-cut: some juvenile
migrants do tend to show compensatory behaviour after displacement when tested
in cages (Åkesson et al.,
2005; Thorup and Rabøl,
2007), and in some species migrations undertaken by juveniles
spread out over large areas and later converge into narrowly defined routes,
the latter also hinting at an ability to navigate in juveniles [e.g. marsh
warblers (Thorup and Rabøl,
2001); Eleonora's falcons
(Gschweng et al., 2008)].
Additionally, the experimental series by Lohmann and Lohmann
(Lohmann and Lohmann, 1994;
Lohmann and Lohmann, 1996a,
Lohmann and Lohmann, 1996b)
show changes in preferred directions as an innate response to experimental
changes in the geomagnetic field by juvenile sea turtles, which could serve a
navigational purpose in keeping inexperienced animals within a goal area.
Hence, at present at least, it cannot be fully ruled out that juveniles have
some sort of innate ability for navigation toward an unknown goal.
Nevertheless, it appears safe to conclude that there is now good evidence that
an experience-based navigation system is important for guiding at least adult
birds to previously experienced wintering and breeding grounds.

Navigation and bi-coordinate maps in migrating animals

The big mystery in our understanding of animal navigation systems still
lies in what the learned navigational system is based upon. GPS and map
location in humans is based on the latitude/longitude coordinate systems. The
current theory of animal navigation is based on a similar system, assuming
extrapolation of familiar gradients to unfamiliar areas
(Fig. 2). If an animal assumes
that a cue with the properties of a gradient (i.e. monotone changes with
distance) varies in the same way outside the home range, such extrapolation
beyond the area in which it is known can be used for navigation.

What cues could be used as gradients? Celestial and magnetic cues have
repeatedly been shown to be important in orientation but their role in bird
navigation remains equivocal despite the fact that both the sun's azimuth and
the strength of the magnetic field are obvious cues to latitude
(Wallraff, 2005). To further
complicate matters, in homing pigeons, evidence indicates that olfactory cues
are necessary for homing from unfamiliar areas
(Gagliardo et al., 2006;
Gagliardo et al., 2008;
Wallraff, 2005). However,
neither current atmospheric models nor navigational map theories explain how
olfactory cues present in Seattle could be detected or used in New Jersey over
3000 km away, as would need to be the case if they were to explain the results
of Thorup et al. (Thorup et al.,
2007).

In a bi-coordinate gradient map animals learn that at least two cues,
ideally intersecting at 90 deg., vary in strength within the home range, and
the animal assumes by extrapolation that they continue to vary in this way
outside the home range. In the case of many long distance migrants, these cues
would need to vary consistently on a global scale, but at the very least on
the basis of current evidence, on a continental scale. In the schematic shown,
if the animal finds itself at A5, B5, then even though it has never
encountered these values in its home range, they are both increasing values.
As gradient A increases northward and gradient B increases westward within the
home range, this means that it is north and west of its home range and must
fly south east to return.

If determining latitude is a relatively easy task, as it is for humans, it
seems reasonable to assume that this is also the case in animals. Indeed, a
number of studies have indicated how animals can recognise latitudinal
displacements. The best evidence for latitudinal cues used in navigation comes
not from migrating birds but from newts, juvenile turtles and lobsters
(Boles and Lohmann, 2003;
Fischer et al., 2001;
Lohmann et al., 2004); all
three studies have indicated that changing the intensity and inclination of
the magnetic field to a value far outside the natural one at the site of
testing results in the animal perceiving its location as latitudinally
displaced. Whether this represents the use of a gradient map to allow
determination of precise latitudinal displacement or a simpler system in which
the animal relies on a rule of thumb to the effect of `when the magnetic field
is greater than the goal, orient southward until it matches the home value'
has not yet been determined as these have not been combined with longitudinal
displacements. More curious is that the distances over which these animals
would normally be required to home are in the region of 10–30 km or
less. Because of local variation in the magnetic field, it has been proposed
that a magnetic map is inoperative or, at best, highly inaccurate over these
distances (Bingman and Cheng,
2006; Phillips et al.,
2006).

Most of the studies on latitudinal displacements refer to species that
normally perform smaller-scale `within home-range' navigation
(Gould, 2004), and we still
lack indications that the mechanisms are the same over longer distances
(thousands of kilometres). Nevertheless, these smaller-scale systems could
provide insights into what could be a possible solution when extending
navigation over longer distances. Due to the general difficulties in
performing these experiments over longer distances, experimenters have often
adhered to very simple designs (and a lack of replication) studying reactions
to single treatments only, which complicates extrapolating the interpretations
of behaviours and increases the chances of misinterpreting behaviours arising
from changes in motivational state for example.

As mentioned previously, the use of a clock, which is independent of local
time, in conjunction with the stars finally allowed humans to solve the
longitude problem. A role of stars in bird orientation was demonstrated early
but whether the stars or the sun are involved in navigation are not well
established. The classic experiment demonstrating a role of the stars in bird
orientation overall indicated the use of stars as a compass in juvenile birds
in that the birds reacted to the axis of celestial rotation, not rotation in
itself (Emlen, 1967), and
studies failing to show compensatory changes of direction over time, which are
not expected if the birds use the stars to navigate, have mostly tested
juveniles in their first migration
(Mouritsen and Larsen, 2001).
And so we can make no conclusion about the role of experience-based maps from
them. Like the stars, the sun can be used to determine longitude, in
conjunction with a clock. When the sunset position has been manipulated by
advancing or delaying the night/day regime (so-called clock shift), birds in
general change direction according to the use of a time-compensated sun
compass, where birds determine a certain compass direction by compensating for
the sun's movement across the sky during the day. In the only sunset test
involving experienced, clock-shifted birds, the birds on northward migration
in spring changed their direction 51 deg. counter-clockwise as a response to a
three hour delayed sunset, approximately in accordance with the 45 deg.
counter-clockwise shift expected from its use as a compass
(Able and Cherry, 1986), and
quite different from the clockwise directional change expected if the birds
perceived the delayed timing as a westward displacement and compensated for
it.

There is also very little direct evidence that magnetic cues are used by
birds to determine latitude in a bi-coordinate map system
(Table 2). Indeed, there are
more reviews published on the subject than there are experiments providing
evidence for the hypothesis at present (reviews by
Bingman and Cheng, 2006;
Freake et al., 2006;
Phillips, 1996;
Wiltschko and Wiltschko, 2006;
Phillips et al., 2006;
Lohmann et al., 2007). A few
studies have dealt with theoretical aspects of whether it is possible to use
the geomagnetic field for navigation (e.g.
Åkesson and Alerstam,
1998) but apart from that there are few studies dealing with
potential coordinates of a map. According to the review by Freake et al.
(Freake et al., 2006), there
is only one direct test of the use of magnetic cues to determine latitude in
migratory birds: a study of Australian silvereyes
(Fisher et al., 2003) showed
northward orientation (towards wintering grounds) when the birds were exposed
to a field with magnetic inclination and intensity corresponding to a location
south of the winter range but when the birds where exposed to magnetic
conditions corresponding to those on the wintering grounds the birds were not
significantly oriented. However, as with the experiments on newts, turtles and
lobsters, the interpretation of the results is still not clear. It could be
the result of recognition of a gradient as part of a map or as a magnetic
`waypoint', i.e. stop migrating when this intensity/inclination is reached. In
another study, involving sea turtles
(Luschi et al., 2007),
individuals with moving magnets attached to their heads showed longer homing
paths than controls, indicating that the birds had to switch to other means of
navigation when the geomagnetic field could not be perceived, but it was not
possible to distinguish between its use in a map or a compass in this
experiment.

Indirect evidence that the magnetic field plays a role in the map of
migratory birds is argued on the basis of the different response between
adults and juveniles in experiments in which a magnetic pulse is administered
(Wiltschko and Wiltschko,
2006). Strong magnetic pulses disrupt magnetite, thought to be
involved in magnetoreception, and it has been demonstrated that adult but not
juvenile birds are affected by these pulses, responding in an orientation cage
by shifting their heading (Munro et al.,
1997). The birds are still able to orient by a magnetic compass
mechanism independent of the magnetite-based sensory system
(Wiltschko et al., 2006),
further suggesting that it could well be a map that is being affected.
However, a property of the pulse experiments may indicate that the
interpretation is only indirect: in some cases birds on both northward and
southward migrations showed eastward migration afterwards
(Wiltschko et al., 1994).
Identical reactions in northward and southward migrations are expected if the
birds perceive the treatment as a displacement but not if the bird's map is
somehow turned (i.e. the direction of a gradient relative to magnetic north).
Recent evidence has indicated that birds also have a magnetite-based fixed
directional response (Stapput et al.,
2008; Wiltschko et al.,
2008) and so further experiments are needed to confirm that the
pulses did not affect this behaviour.

In contrast to the studies indicating the magnetic field to be part of the
navigational map, two studies on albatrosses aimed at testing whether magnetic
cues are involved in navigation failed to find an effect: homing albatrosses
with magnets attached to their heads behaved similarly to control birds
without magnets (Bonadonna et al., 2007;
Mouritsen et al., 2003).
However, failure to demonstrate an effect of a sensory manipulation does not
represent evidence for rejection of that sense as a navigational cue
(Freake et al., 2006) and so
what such studies mean is unclear, although they certainly demonstrate that
magnetic cues do not represent the only means by which long-distance
navigators can determine position. On this note, despite a large body of
evidence that indicates that olfactory cues play a role in the successful
homing of pigeons (Papi, 2001;
Wallraff, 2005), little
attention has been given as to what role, if any, olfactory cues might play in
migratory navigation. The instability of the atmosphere over terrestrial
locations would seem to make it unlikely that olfaction would play any role in
a global scale bi-coordinate map, either as a longitudinal or latitudinal cue
(Bingman and Cheng, 2006), but
it has been proposed that it may play a role, in conjunction with the
inherited migratory direction, in successful migration
(Wallraff, 2005). In a marine
environment, large stable odour plumes made up from dimethylsulphide (DMS)
make it possible that olfactory cues could play a role in a map
(Nevitt and Bonadonna, 2005).
These hypotheses have not so far been tested however.

As this shows, the evidence for the use of a long-range bi-coordinate map
in animals is still rather scant. However, it is not given that animals rely
solely on a bi-coordinate map. The map could easily be multi-coordinate, and
two studies hint at the possibility of the additional use of inherited
magnetic `signposts': young pied flycatchers changed direction according to
shifts in the magnetic field simulating the shifts experienced along the
migratory route (Beck and Wiltschko,
1982; Beck and Wiltschko
1988), and fat deposition in young thrush nightingales was
similarly affected by changes in the magnetic field
(Fransson et al., 2001).

The way forward?

In conclusion, we have a number of exciting experiments pointing to
possible ways that long-distance navigation may work but we need many more
experiments before we can conclude that a bi- or perhaps multi-coordinate map
underlies experience-based long-distance navigation by migratory birds. It is
beyond reasonable doubt that many birds are able to locate their direction of
displacement precisely and over long distances. This must be achieved by an
experience-based system, which appears in some cases at least to have
near-global coverage. Likely candidates for this map are celestial,
geomagnetic and possibly even olfactory but we cannot be as sure that a
bi-coordinate latitude/longitude map is the best model for this system. Very
few studies of migratory birds in a natural setting have been performed. While
experiments in controlled conditions are necessary to titrate fine scale
details of behaviour (Freake et al.,
2006), knowledge is almost entirely lacking in the study of bird
migration of the nature of the cues essential for navigation in the wild.

We suggest that the way forward is to `go wild' – extending research
on long-distance migratory birds into a natural setting
(Wikelski et al., 2007), where
it has so far mostly been carried out in cages. However, this must go
hand-in-hand with a lab-based effort to study many species and situations to
solve this complicated issue. In most laboratory studies, animals move
distances of only few decimetres as maximum. Relating this behaviour to the
situation in the wild, where conditions change vastly might be difficult.
Although a good deal of understanding can no doubt come from field-based
research on homing pigeons, we still have hardly explored how animals actually
behave over long-distance migrations.

Orientation cage experiments and homing pigeon research have provided a
wealth of data, yet several examples demonstrate how field-based research
might further or change our understanding of the results obtained in the
laboratory. For example, a recent field tracking study of migrating thrushes
demonstrated the sunset as the primary calibration cue
(Cochran et al., 2004), in
contrast to the many laboratory studies indicating the magnetic compass as the
primary calibration cue (Wiltschko and
Wiltschko, 1995).

We believe that repeating many of the findings from the laboratory in the
wild will provide clues to a deeper understanding of the behaviours observed
so far. Additionally, our current inability to track smaller migrants over
longer distances has left us somewhat unsure of the true capabilities of wild
birds under natural migrations, which might be different to what has been
established so far for long-distance migrants, mostly from movements of a few
centimetres in a laboratory.

Glossary

Clock shift

Advancing or delaying the night/day regime. If birds are kept indoors in
artificial light, the night/day regime is easily advanced or delayed. For
example, if the sunrise and sunset positions advanced by three hours compared
with the local light regime, the bird's internal clock will be three hours
ahead when the bird is exposed to the natural light regime.

Gradient map

A map based on cues, which vary predictably with gradients as shown in
Fig. 2. The cues can be used to
determine the coordinates in a map and then to calculate the direction toward
a goal with known coordinates in the gradient system. Such a direction need
not be calculated precisely but could be of the type `fly southeast', if the
experienced cue values are to the north and west of its home. Continuously
monitoring the gradient values will ensure returning home even though the path
will not be direct.

GPS

Global Positioning System. A satellite system enabling the determination of
ones location (latitude, longitude and altitude) with an accuracy in the order
of less than 10 m anywhere on earth using a GPS receiver.

Home range navigation

Finding the way in a well-known area, typically the normal home range.

Homing

Homing is the process of returning accurately to a known, previously
visited location from a distance. To successfully home from unfamiliar
territory one needs to navigate.

Migration

Migration can refer to a more or less permanent movement of an animal away
from an area, which the animal is using on a daily basis, for instance the
area around a nesting site. Here, we will however mostly be concerned with the
seasonal movement of animals back and forth between breeding and wintering
grounds.

Navigation

For practical reasons, we will make a clear distinction between navigation
and orientation. Navigation is the process of finding a goal whereas
orientation involves only the ability to take up a particular direction. Thus,
navigation allows correction for displacements whereas the latter does not.
This distinction is crucial in animal orientation/navigation studies.

Orientation

The process of orientation concerns the ability to determine a compass
direction. Thus, no ability to find a goal is involved. Orientation can also
refer to the direction of movement.

Time-compensated sun compass

A time-compensated sun compass uses the azimuth of the sun to determine
compass directions, compensating for the sun's movement across the sky during
the day, i.e. knowing how fast it moves (approximately 15 deg. per hour).